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The Control of Metabolic Traits by Octopamine and Tyramine in Invertebrates Thomas Roeder1,2,*

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The Control of Metabolic Traits by Octopamine and Tyramine in Invertebrates Thomas Roeder1,2,* © 2020. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2020) 223, jeb194282. doi:10.1242/jeb.194282 REVIEW The control of metabolic traits by octopamine and tyramine in invertebrates Thomas Roeder1,2,* ABSTRACT recently questioned (Bauknecht and Jékely, 2017). The authors α β Octopamine (OA) and tyramine (TA) are closely related biogenic claim that - and -adrenergic receptors as well as OA and TA monoamines that act as signalling compounds in invertebrates, receptors were part of the ancestral receptor repertoire of primordial where they fulfil the roles played by adrenaline and noradrenaline in metazoans; therefore, final clarification of this issue is still pending. vertebrates. Just like adrenaline and noradrenaline, OA and TA are Finally, similarities in these systems also exist at the level of the ‘ extremely pleiotropic substances that regulate a wide variety of physiological processes that they control. The famous fight-or- ’ processes, including metabolic pathways. However, the role of OA flight response, which is activated in vertebrates by adrenaline and/ and TA in metabolism has been largely neglected. The principal aim or NA, and in invertebrates by OA and TA, is the most obvious of this Review is to discuss the roles of OA and TA in the control of example of these physiological similarities. Fight-or-flight metabolic processes in invertebrate species. OA and TA regulate responses use adrenaline/NA or TA/OA to induce the relevant essential aspects of invertebrate energy homeostasis by having physiological effects, but they are also characterised by complex substantial effects on both energy uptake and energy expenditure. regulatory inputs that enable their efficient execution. For example, These two monoamines regulate several different factors, such as in vertebrates, the bone-derived osteocalcin system suppresses metabolic rate, physical activity, feeding rate or food choice that have parasympathetic activities in response to fear, thus strengthening the a considerable influence on effective energy intake and all the fight-or-flight response (Berger et al., 2019). principal contributors to energy consumption. Thereby, OA and TA Numerous studies have shown the regulatory effects of TA and, ’ regulate both metabolic rate and physical activity. These effects especially, OA on almost all aspects of an animal s life, and a should not be seen as isolated actions of these neuroactive number of comprehensive reviews summarise these data (Chase and compounds but as part of a comprehensive regulatory system that Koelle, 2007; Roeder, 1999, 2005; Roeder et al., 2003). However, allows the organism to switch from one physiological state to another. there has been relatively little progress in the differentiation of the effects of OA and TA to date. In some systems, opposing effects of KEY WORDS: Drosophila melanogaster, Noradrenaline, these substances have been identified, which implies that the Caenorhabditis elegans, Metabolism various functions may be regulated differently according to the proportions of OA and TA present (Alkema et al., 2005; Damrau Introduction et al., 2018; Saraswati et al., 2004; Vierk et al., 2009). These specific Octopamine (OA) and tyramine (TA) are biogenic amines that are and, in some cases, antagonistic effects of OA and TA will be derived from the amino acid tyrosine and are of the utmost discussed in different parts of this Review. For TA, a particular role importance in invertebrates. These neuroactive substances fulfil the as a neuroactive substance has been highlighted in a number of physiological roles that adrenaline and noradrenaline (NA) perform studies and reviews (Blenau and Baumann, 2003; Cazzamali et al., in vertebrates (Roeder, 1999, 2005). Like adrenaline and NA, both 2005; Lange, 2009; Roeder et al., 2003). However, what at first OA and TA are highly pleiotropic – they are involved in regulating a glance appears to be a surprising variety of effects, largely induced wide range of behaviours, physiological variables and, more by OA, merges into a coherent overall picture on closer inspection. specifically, metabolic pathways. Similarities exist between these In most instances, OA seems to be the messenger that coordinates two signalling systems in invertebrates and vertebrates at various the activities of a number of organs, orchestrating a change from a levels. First, it should be noted that these signalling substances have resting state to a state of higher activity. This concerted action strikingly similar structures: NA differs from OA only in the involves behavioural changes, metabolic adjustments and the presence of an additional hydroxyl group at position three of the optimisation of the performance of various organ systems phenolic ring (Roeder, 1999; Roeder et al., 2003). Furthermore, TA (Adamo et al., 1995; Stevenson and Rillich, 2012). The processes is the biological precursor of OA and adrenaline is produced from that are regulated in this way include those that require substantial NA; thus, each signalling system comprises two messenger resources, such as egg laying (Avila et al., 2012; Lee et al., 2003; Li substances that are not completely independent of one another. et al., 2015). The respective receptors, the α- and β-adrenergic receptors of Central to the combined actions of OA are effects on the vertebrates and the OA and TA receptors of invertebrates, also share circulation, with changes in the heart rate being the most important substantial sequence similarity, suggesting that they have common outcome. Effects of OA, but also of TA, on heart rate have been evolutionary origins (Fig. 1). However, this interpretation was reported for a number of different species (Fig. 2). In most cases, these amines act to increase the heart rate, whereas for some 1Kiel University, Zoology, Department of Molecular Physiology, 24098 Kiel, preparations an inhibitory effect has been shown (Chowanski et al., Germany. 2DZL, German Centre for Lung Research, ARCN, 24098 Kiel, Germany. 2017; Papaefthimiou and Theophilidis, 2011; Pryce et al., 2015). Increased heart rate makes all exchange processes more efficient. *Author for correspondence ([email protected]) Graham Hoyle proposed a hypothesis that describes OA as a T.R., 0000-0002-3489-3834 messenger compound that modulates a number of different Journal of Experimental Biology 1 REVIEW Journal of Experimental Biology (2020) 223, jeb194282. doi:10.1242/jeb.194282 most important components of energy expenditure, namely Glossary metabolic rate (see Glossary) and physical activity (Fig. 3). Circadian clocks Whenever information is available, I will discuss the effects of Most animals have a circadian rhythm that is controlled by a central the two monoamines separately. circadian clock, which enables the maintenance of rhythm even in the absence of external Zeitgebers (‘time-givers’). Peripheral clocks are Control of hunger, satiety and food selection present in a number of different peripheral organs to regulate local circadian processes. The control of food intake is of central importance to all metabolic Cytoprotective response processes because it regulates the supply of energy. This means that A response induced in cells after exposure to stress that increases the interaction of hunger and satiation, and the resulting regulation cellular stress resistance. Hunger and reduced food intake are among of food intake, is of great significance when considering the most important inducers of a cytoprotective response. This response metabolism. OA has numerous physiological effects that are is characterised by the induced expression of a defined set of genes. important during a period of hunger. Hunger triggers the release Lipolysis The process of releasing fatty acids from storage triglycerides present in of OA, which induces a suitable physiological response (Tao et al., storage organs (fat bodies in insects, intestinal cells in nematodes). This 2016). Early studies revealed that the administration of exogenous release is necessary to provide energy when needed and is regulated by OA phenocopies the effects of starvation in Caenorhabditis elegans hormones. (Horvitz et al., 1982), and higher body concentrations of OA have Metabolic rate been observed during starvation – Tao and colleagues (2016) The metabolic activity and associated energy consumption that occur in reported a 3–4 times higher OA concentration in fasted C. elegans the absence of physical activity in an organism. It is one of the major components contributing to the overall energy expenditure. compared with well-fed ones. Mushroom bodies (corpora pedunculata) Invertebrates have evolved a number of different strategies to Regions in the insect (arthropod) brain that have a mushroom-like prevent starvation. Starvation activates behavioural responses aimed appearance. The structure is mainly made of fibres of so-called Kenyon at increasing food intake. During starvation, food availability, rather cells and it is known to play a central role in olfactory learning and than the capacity for feeding, is usually the limiting factor. memory. Therefore, movement to locate new food sources is an appropriate Neurohormones response. Consequently, starvation-induced behavioural responses Messenger compounds that are produced by neurons and reach their target organs via the blood/body fluid. Tyramine and octopamine as well include greater locomotor activity. In D. melanogaster, this as adrenaline and noradrenaline are classic neurohormones, as
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